Evolution of complex life cycles in helminth parasites (original) (raw)

Nature volume 425, pages 480–484 (2003)Cite this article

Abstract

The fundamental question of how complex life cycles—where there is typically more than one host—evolve in host–parasite systems remains largely unexplored. We suggest that complex cycles in helminths without penetrative infective stages evolve by two essentially different processes, depending on where in the cycle a new host is inserted. In ‘upward incorporation’, a new definitive host, typically higher up a food web and which preys on the original definitive host, is added. Advantages to the parasite are avoidance of mortality due to the predator, greater body size at maturity and higher fecundity. The original host typically becomes an intermediate host, in which reproduction is suppressed. In ‘downward incorporation’, a new intermediate host is added at a lower trophic level; this reduces mortality and facilitates transmission to the original definitive host. These two processes should also apply in helminths with penetrative infective stages, although the mathematical conditions differ.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. Roff, D. A. The Evolution of Life Histories: Theory and Analysis (Chapman & Hall, New York, 1992)
    Google Scholar
  2. Kozlowski, J. Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7, 15–19 (1992)
    Article CAS Google Scholar
  3. Charnov, E. L. Life History Invariants (Oxford Univ. Press, Oxford, 1993)
    Google Scholar
  4. Gemmill, A. W., Skorping, A. & Read, A. F. Optimal timing of first reproduction in parasitic nematodes. J. Evol. Biol. 12, 1148–1156 (1999)
    Article Google Scholar
  5. Poulin, R. Evolutionary Ecology of Parasites (Chapman & Hall, London, 1998)
    Google Scholar
  6. Poulin, R. & Cribb, T. H. Trematode life cycles: short is sweet? Trends Parasitol. 18, 176–183 (2002)
    Article Google Scholar
  7. Brown, S. P., Renaud, F., Guegan, J. F. & Thomas, F. Evolution of trophic transmission in parasites: the need to reach a mating place? J. Evol. Biol. 14, 815–820 (2001)
    Article Google Scholar
  8. Redi, F. Experimenta circa generationem insectorum, ad nobilissimum vivum Carolum Dati (Amstelodami, 1671)
    Google Scholar
  9. Eberman, B. Evolution in organisms that change their niches during the life-cycle. Am. Nat. 139, 990–1021 (1992)
    Article Google Scholar
  10. Price, P. W. Evolutionary Biology of Parasites (Princeton Univ. Press, Princeton, 1980)
    Google Scholar
  11. Esch, G. W. & Fernández, J. C. A Functional Biology of Parasitism (Chapman & Hall, London, 1993)
    Book Google Scholar
  12. Morand, S., Robert, F. & Connors, V. A. Complexity in parasite life cycles: population biology of cestodes in fish. J. Anim. Ecol. 64, 256–264 (1995)
    Article Google Scholar
  13. Baer, J. G. Ecology of Animal Parasites (Univ. Illinois Press, Urbana, 1952)
    Google Scholar
  14. Moravec, F. Parasitic Nematodes of Freshwater Fish in Europe (Academic/Kluwer, Prague/Dordrecht, 1994)
    Google Scholar
  15. Harvey, P. H. & Keymer, A. E. Comparing life histories using phylogenies. Phil. Trans. R. Soc. Lond. B 332, 31–39 (1991)
    Article ADS Google Scholar
  16. Morand, S. Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Funct. Ecol. 10, 210–218 (1996)
    Article Google Scholar
  17. Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. & Milinski, M. Optimal growth strategies of larval helminths in their intermediate hosts. J. Evol. Biol. 16, 47–54 (2003)
    Article CAS Google Scholar
  18. Nickol, B. B. in Biology of the Acanthocephala (eds Crompton, S. W. T. & Nickol, B. B.) (Cambridge Univ. Press, Cambridge, 1985)
    Google Scholar
  19. Mackiewicz, J. S. Caryophyllidea (Cestoidea): a review. Exp. Parasitol. 31, 417–512 (1972)
    Article CAS Google Scholar
  20. Wisniewski, L. W. Cyathocephalus truncatus Pallas. II. Allgemeine Morphologie. Bull. Int. Acad. Polon. Sci. Lett. Cracovie. Class Sci. Math. Nat. B 3, 311–327 (1933)
    Google Scholar
  21. Anderson, R. C. Nematode Parasites of Vertebrates 2nd edn (CABI, Wallingford, 2000)
    Book Google Scholar
  22. Matsuno, K. & Ohno, N. How many trophic levels are there? J. Theor. Biol. 180, 105–109 (1996)
    Article Google Scholar
  23. Briand, F. & Cohen, J. E. Environmental correlates of food chain length. Science 238, 956–960 (1987)
    Article ADS CAS Google Scholar
  24. Stunkard, H. W. Interrelationships and taxonomy of the digenetic trematodes. Biol. Rev. 21, 148–158 (1946)
    Article CAS Google Scholar
  25. Brooks, D. R. & McLennan, D. A. Parascript: Parasites & the Language of Evolution (Smithsonian Institution, Washington, 1993)
    Google Scholar
  26. Molnár, K. Bothriocephalus phoxini sp. N. (Cestoda, Pseudophyllidea) from Phoxinus phoxinus L. Folia Parasitol. 14, 83–86 (1968)
    Google Scholar

Download references

Acknowledgements

We thank the NERC for funding. Pilot versions of some of these ideas were first analysed by G.A.P. while supported by a Nuffield Research Fellowship in 1983.

Author information

Authors and Affiliations

  1. Population and Evolutionary Biology Research Group, School of Biological Sciences, University of Liverpool, L69 7ZB, Liverpool, UK
    Geoff A. Parker, Jimmy C. Chubb & Guy N. Roberts
  2. Division of Applied Mathematics, Department of Mathematical Sciences, University of Liverpool, L69 3BX, Liverpool, UK
    Michael A. Ball

Authors

  1. Geoff A. Parker
  2. Jimmy C. Chubb
  3. Michael A. Ball
  4. Guy N. Roberts

Corresponding author

Correspondence toGeoff A. Parker.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

About this article

Cite this article

Parker, G., Chubb, J., Ball, M. et al. Evolution of complex life cycles in helminth parasites.Nature 425, 480–484 (2003). https://doi.org/10.1038/nature02012

Download citation

This article is cited by